Methanogenesis in phytotelmata: Microbial communities and methane cycling in bromeliad tanks and leaf axils of oil palms
The global emission of methane (CH4) is estimated to be 500-600 Tg per year from diverse natural and man-made sources. Wetlands are the main source of methane and provide an ideal habitat for anaerobic methanogenic archaea which significantly contribute to the total global methane emission. Besides...
|PDF Full Text
No Tags, Be the first to tag this record!
|The global emission of methane (CH4) is estimated to be 500-600 Tg per year from diverse natural and man-made sources. Wetlands are the main source of methane and provide an ideal habitat for anaerobic methanogenic archaea which significantly contribute to the total global methane emission. Besides permanently flooded wetlands, there are distinct wetlands created by small water bodies within parts of plants, called phytotelmata. These water catchments in tropical forests comprise bamboo nodes, pitcher plants, tree holes, tank bromeliads and non-bromeliads leaf axils. Recent work indicates that phytotelmata may contribute to the global methane budget. Tank bromeliads, which effectively collect rainwater and organic substrate between their leaf axils (tank slurry), emit substantial amounts of methane into the atmosphere over neotropical forests. However, studies on the microbial communities involved in methane cycling and environmental factors which influence their activity are still rare. In the present study we established tank bromeliads as a model system in the greenhouse and collected field data to investigate the microbial communities in tank bromeliads.
Investigation of Costa Rican tank bromeliads revealed that inhabiting microbial communities (Bacteria, Archaea) differed between individual plants, although the plants belong to the same species and were growing in the same habitat patch. Major determinants for the individual plants microbial community composition were carbon, nitrogen, oxygen concentrations, and the pH of tank slurries. These factors depend on the incoming rainwater, leaf litter or input by higher organisms (e.g. insects, spiders, birds). Therefore, the site where a tank bromeliad develops may play an important role for the inhabiting microbial communities. In summary, our results indicate that every bromeliad tank is a unique island with respect to its resident microbial community. The presence of methanogens and methanotrophs in all tank slurries further indicates the potential for both methane formation and methane oxidation in the bromeliad tanks.
Besides tank slurry properties we have shown that the availability of water shapes the archaeal and bacterial community in tank bromeliads. Increasing drought resulted in a decrease of methane formation and in a shift from a hydrogenotrophic dominated community (Methanobacteriales) to an aceticlastic (Methanosaetaceae) dominated methanogenic community. This trend was also observed in the isotopic signature of produced methane and so hydrogenotrophically derived methane dominated under high moisture. Increasing drought resulted in increasing oxygen exposure for the microoorganisms. We found genes for oxygen detoxifying enzymes in genomes of Methanosaeta species, indicating that these methanogens are more oxygen tolerant than previously assumed. With increasing drought the relative abundance of the Burkholderiales, mainly represented by the genus Burkholderia, more than tripled in tank slurry whereas the bacterial diversity decreased. Furthermore, regardless of the water content or the incubation environment (inside or outside of bromeliad tanks) the genus Burkholderia was the most abundant group, indicating its tolerance towards changing water levels which frequently occur in tank bromeliads under natural conditions. Upon drought gene copy numbers of nifH, a marker gene for nitrogen fixation known to occur in Burkolderia spp. as well as Methanosaeta spp., increased. Therefore, this work indicates that tank bromeliads inhabiting microbes are not only involved in carbon cycling but also in nitrogen cycling.
We further investigated the potential of methane formation in non-bromeliad leaf axils. The leaf axils of oil palms create catchments similar to the leaf axils of tank bromeliads where organic matter and rainwater accumulate. In incubation experiments we showed that under water-logged oxic or anoxic conditions methane is formed in this organic material, accompanied by increasing gene copy numbers of mcrA, a commonly used marker gene for methanogens. Therefore, our results indicate that leaf axils of oil palms seem to be a potential habitat for methanogenesis.
The results of this work give new insights into the microbial communities and methane cycling in plant leaf axils and emphasize the need to better resolve the role of phytotelmata in the cycling of methane to better understand the global methane budget.